FLIES INFECTED BY ENTOMOPATHOGENIC FUNGI IN
Transcrição
FLIES INFECTED BY ENTOMOPATHOGENIC FUNGI IN
bioRxiv preprint first posted online Nov. 25, 2014; doi: http://dx.doi.org/10.1101/011742. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. 1 1 FLIES INFECTED BY ENTOMOPATHOGENIC FUNGI IN AN URBAN FRAGMENT 2 OF SEMIDECIDUOUS FOREST 3 4 Bruno Corrêa Barbosa¹*, Tatiane Tagliatti Maciel¹, Fábio Prezoto¹ 5 (1) Laboratório de Ecologia Comportamental e Bioacústica (LABEC), Universidade Federal de Juiz 6 de Fora, Juiz de Fora, Minas Gerais, Brasil. E-mail: [email protected] 7 8 Abstract: Entomopathogenic fungi parasitize a wide variety of hosts may be involved in regulating 9 the populations of these arthropods helping maintain stability in tropical forest ecosystems. The 10 genus Ophiocordyceps and Entomophthora contains several species of entomopathogenic fungi 11 specialized to infect and kill their hosts due to development and the need for transmission by 12 manipulating host behavior. Despite mounting research in the area, works with parasitized flies are 13 scarce. This study aims to describe associations between the occurrence of entomopathogenic fungi 14 and parasitic flies of the family Muscidae and behaviors presented by these flies parasitized in an 15 urban fragment of semideciduous forest in southeastern Brazil. Were recorded two species of 16 entomopathogenic fungi parasitizing flies collected for the first time in this locality, E. muscae and 17 O. dipterigena. Different from Diptera parasitized by different fungi behaviors were observed. 18 These new records of occurrence, along with data on their hosts, suggest that many species of this 19 group have not yet registered. Therefore, more studies in tropical forests will certainly increase the 20 knowledge about these interactions. 21 22 Keywords: Entomophthora, fungal diversity, Muscidae, Ophiocordyceps, parasite manipulation. 23 24 INTRODUCTION 25 The entomopathogenic fungi parasitizing a wide variety of hosts (SAMSON & EVANS 1982, 26 1984; KOBAYASI 1941) and may change their behavior in order to favor the dispersion of the 27 manipulator (ANDERSEN et al. 2009). There are records of infection of these fungi in eleven insect 28 orders: Hymenoptera, Diptera, Coleoptera, Hemiptera, Lepidoptera, Orthoptera, Isoptera, Blattodea, 29 Odonata, Mantodea and Dermaptera, and other arthropods such as spiders (EVANS 1982). It is 30 believed that these fungi are involved in regulating the populations of these arthropods may help 31 maintain stability in the tropical forest ecosystems (EVANS 1982). 32 The genus Ophiocordyceps and Entomophthora contains several species of 33 entomopathogenic fungi specialized to infect and kill their hosts due to a development and 34 transmission necessity (STEENBERG et al. 2001; EVANS et al. 2011). Some species, such as 35 Ophiocordyceps unilateralis sensu lato, are capable to manipulate the host’s behavior, causing it to bioRxiv preprint first posted online Nov. 25, 2014; doi: http://dx.doi.org/10.1101/011742. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. 2 1 abandon the colony and act in detriment to its own to enhance the parasite’s fitness (ANDERSEN et 2 al. 2009). This behavior, in which genes of the parasite are expressed in the host’s phenotype, may 3 be classified as an extended phenotype (DAWKINS 1982). 4 Due to the high abundance, fungal infections in Formicidae are the most reported and most 5 well known. The infection occurs during foraging when the ants come into contact with the spores 6 that get stuck in their body and penetrate their cuticle. The period of the fungus infection occurs 7 within three to six days after spore adhesion of the body surface ant. Once infected, an individual 8 dies and the fungus produces a fruiting body that grows just behind the head of the parasitized 9 insect. For this structure, the fungus produces spores that are dispersed across the forest floor, where 10 they, infect new hosts (EVANS 1982; EVANS & SAMSON 1982, 1984; PONTOPPIDAN et al. 2009). 11 On the other hand, records the occurrence of infection of entomopathogenic fungi in Diptera 12 are scarce, as well as information about the behavioral changes caused by the fungus and their 13 hosts. Thus, this study describes the occurrence of parasitic associations between entomopathogenic 14 fungi and flies of the family Muscidae and a brief description of their behavior in an urban fragment 15 of Atlantic rainforest in southeastern Brazil. 16 17 METHODS AND MATERIALS 18 Records occurred in 2014 and were held in the Botanical Garden of the Federal University 19 of Juiz de Fora (21 ° 43 '28 "S - 43 ° 16' 47" W), a fragment of Semideciduous Seasonal Forest 20 Montana (VELOSO et al. 1991) recently classified by SANTIAGO et al. (2014) as expressive richness, 21 diversity and floristic diversity of woody vegetation, with endangered species with predominance of 22 pioneer plant complex, besides the considerable presence of exotic species. The area of 84 hectares 23 of extension is located within the city limits of Juiz de Fora, southeastern state of Minas Gerais, 24 Brazil (Figure 1), 750 m above sea featuring warm subtropical climate with dry winter and wet 25 summer level (Cwa), according to the classification of Köppen (SÁ-JUNIOR 2009). 26 Fungi were also identified by Prof. Harry Evans, CABI and João Paulo Machado de Araujo 27 of Pennsylvania State University, based on morphological analysis of fruiting bodies and 28 identification of the hosts present. 29 bioRxiv preprint first posted online Nov. 25, 2014; doi: http://dx.doi.org/10.1101/011742. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. 3 1 2 Figure 1: Location of the Botanical Garden of the Federal University of Juiz de Fora, Brazil. 3 4 RESULTS AND DISCUSSION 5 Two species of entomopathogenic fungi were collected for the first time in this locality, 6 Entomophthora muscae (Cohn) Fresen. (Figure 2a and 2b) and Ophiocordyceps dipterigena (Berk. 7 & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora (Figure 2c and 2d) with host on adult 8 of Diptera (Muscidae). 9 Due to the effect of partial decomposition caused by the fungus, the identification of Diptera 10 were only possible family level (Muscidae) for the individual parasitized by Ophiocordyceps 11 dipterigena and gender (Musca sp) for the individual parasitized by Entomophthora muscae. 12 In this study, fungal species showed distinct forms as the manipulation of the setting 13 behavior where E. muscae seems to control the fly in looking for a vine leaf, and with his legs cling, 14 favoring for development the fungus. It was observed that the fungus monopolize the entire surface 15 of the fly between the membranes including the abdominal segments, mesossomal and sclerites 16 (Figure 2a and 2b). The species O. dipterigena seems manipulate the insect to land on a sheet bioRxiv preprint first posted online Nov. 25, 2014; doi: http://dx.doi.org/10.1101/011742. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. 4 1 without the need to hold her where, after the death of the fly, the fruiting body emerges, 2 extrapolated the body of the fly, getting out of the inside through the head (Figure 2c and 2d). 3 As data on these parasitic associations are still rare, especially in anthropogenic areas 4 (TRAVIS et al. 1993; LASTRA et al. 2006; SUNG et al. 2007), these new records of occurrence, along 5 with data on their hosts, suggest that many species of this group have not yet registered. Therefore, 6 more studies in tropical forests will certainly increase the knowledge about these interactions. 7 8 9 Figure 2: Flies infected by entomopathogenic fungi found in the Botanical Garden of the Federal 10 University of Juiz de Fora: A and B - Fly parasitized by Entomophthora muscae; C and D - Fly 11 parasitized by Ophiocordyceps dipterigena. 12 13 REFERENCES 14 Andersen, S.B., S. Gerritsma, K.M., Yusah, D., Mayntz, N.L., Hywel-Jones, J., Billen, J.J. 15 Boomsma & D.P., Hughes, 2009. The life of a dead ant: the expression of an adaptive extended 16 phenotype. The American Naturalist, 174: 424-33. 17 Dawkins, R., 1982. The Extended Phenotype. Oxford (UK): Oxford University Press., 307 p. 18 Evans, H.C. & R.A., Samson, 1984. Cordyceps species and their anamorphs pathogenic on ants 19 (Formicidae) in tropical forest ecosystems II. The Camponotus (Formicinae) complex. Transactions 20 of the British Mycological Society, 82: 127-150. bioRxiv preprint first posted online Nov. 25, 2014; doi: http://dx.doi.org/10.1101/011742. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. 5 1 Evans, H.C., 1982. Entomogenous fungi in the tropical forest ecosystems: na appraisal. Ecological 2 Entomology, 7: 47-60. 3 Evans, H.C., S.L., Elliot & D.P., Hughes, 2011. Hidden diversity behind the zombie-ant fungus 4 Ophiocordyceps unilateralis: four new species described from carpenter ants in Minas Gerais, 5 Brazil. PLoS ONE, 6: e17024. 6 Lastra, C.C.L., A., Siri, J.J., García, J., Eilenberg & R.A., Humber, 2006. Entomophthora 7 ferdinandii (Zygomycetes: Entomophthorales) causing natural infections of Musca domestica 8 (Diptera: Muscidae) in Argentina. Mycopathologia 161: 251-254. 9 Pontoppidan, M.B., W., Himaman, N.L., Hywel-Jones, J.J., Boomsma & D.P., Hughes, 2009. 10 Graveyards on the move: the spatio-temporal distribution of dead Ophiocordyceps-infected ants. 11 PLoS ONE 4: e4835. 12 Sá Júnior, A., 2009. Aplicação da classificação de Köppen para o zoneamento climático do estado 13 de Minas Gerais. Dissertação (Ph.D. em Engenharia Agrícola) - Universidade Federal de Lavras, 14 101 p. 15 Santiago, D.S., C.R. da Fonseca & F.A., Carvalho, 2014. Fitossociologia da regeneração natural de 16 um fragmento urbano de Floresta Estacional Semidecidual (Juiz de Fora, MG). Revista Brasileira 17 de Ciências Agrárias, 9: 117-123. 18 Steenberg, T., J.B., Jespersen, K.M.V., Jensen, B.O., Nielsen & R.A., Humbert, 2001. 19 Entomopathogenic fungi in flies associated with pasture cattle in Denmark. Journal of Invertebrate 20 Pathology, 77: 186–197. 21 Sung, G.H., N.L., Hywell-Jones, J.M., Sung, J.J., Luangsa-ard, B., Shrestha & J.W., Spatafora. 22 2007. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology, 23 57: 5-59. 24 Travis, R.G., M., O'Callaghan & P.J., Wigley, 1993. Checklist of naturally occurring 25 entomopathogenic microbes and nematodes in New Zealand, New Zealand Journal of Zoology, 20: 26 95-120. 27 Veloso, H.P., A.L.R., Rangel-Filho & J.C.A. Lima, 1991. Classificação da vegetação brasileira 28 adaptada a um sistema universal. Rio de Janeiro: IBGE, 124p.
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